Comparative genomics and the nature of placozoan species
Michael Eitel , Warren R. Francis, Frédérique Varoqueaux, Jean Daraspe, Hans-Jürgen Osigus, Stefan Krebs, Sergio Vargas, Helmut Blum, Gray A. Williams, Bernd Schierwater, Gert Wörheide
Published: July 31, 2018 https://doi.org/10.1371/journal.pbio.2005359
Abstract
Placozoans are a phylum of nonbilaterian marine animals currently represented by a single described species, Trichoplax adhaerens, Schulze 1883. Placozoans arguably show the simplest animal morphology, which is identical among isolates collected worldwide, despite an apparently sizeable genetic diversity within the phylum. Here, we use a comparative genomics approach for a deeper appreciation of the structure and causes of the deeply diverging lineages in the Placozoa. We generated a high-quality draft genome of the genetic lineage H13 isolated from Hong Kong and compared it to the distantly related T. adhaerens. We uncovered substantial structural differences between the two genomes that point to a deep genomic separation and provide support that adaptation by gene duplication is likely a crucial mechanism in placozoan speciation. We further provide genetic evidence for reproductively isolated species and suggest a genus-level difference of H13 to T. adhaerens, justifying the designation of H13 as a new species, Hoilungia hongkongensis nov. gen., nov. spec., now the second described placozoan species and the first in a new genus. Our multilevel comparative genomics approach is, therefore, likely to prove valuable for species distinctions in other cryptic microscopic animal groups that lack diagnostic morphological characters, such as some nematodes, copepods, rotifers, or mites.
Author summary
Placozoans are a phylum of tiny (approximately 1 mm) marine animals that are found worldwide in temperate and tropical waters. They are characterized by morphological simplicity, with only a handful of cell types, no neurons, no tissue organization, and even no axial polarity. Since the original description of Trichoplax adhaerens 135 years ago, no additional accepted species has been established, leaving the Placozoa as the only animal phylum with only a single formally described species. While classical morphological species identification has failed to reveal further species, single-gene DNA sequence analyses have identified a broad and deep genetic diversity within the Placozoa. To address the significance of this deep genetic diversity in this morphologically uniform phylum, and to better understand its consequences for speciation processes, general biology, and species delimitation in the Placozoa, we sequenced the genome of the placozoan isolate “H13,” a lineage distantly genetically related to T. adhaerens. Our multilevel genomic comparisons with the T. adhaerens genome show considerable differences in the general structure of the genome and the makeup and history of various gene families of biological relevance to habitat adaptation. Based on comparative genomics, we here describe the second placozoan species and show that it belongs to a new genus.
Citation: Eitel M, Francis WR, Varoqueaux F, Daraspe J, Osigus H-J, Krebs S, et al. (2018) Comparative genomics and the nature of placozoan species. PLoS Biol 16(7): e2005359. https://doi.org/10.1371/journal.pbio.2005359
Academic Editor: Chris Tyler-Smith, The Wellcome Trust Sanger Institute, United Kingdom of Great Britain and Northern Ireland
Received: January 5, 2018; Accepted: June 28, 2018; Published: July 31, 2018
Copyright: © 2018 Eitel et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Python scripts used in this study are available at https://bitbucket.org/wrf/sequences and https://github.com/wrf/lavaLampPlot. Raw genomic short and long reads, as well as RNA-Seq reads, respectively, have been deposited at NCBI Short Read Archive under SRR5311040, SRR5311137, SRR5311041. Bioproject accession is PRJNA377631. A repository has been created that hosts all files related to the genome and performed analyses (https://bitbucket.org/molpalmuc/hoilungia-genome): Masked and unmasked reference genome assembly [fasta] Transcriptome and proteome versions [fasta] Annotation tracks [GFF]: genes, CDS, mapped transcripts, SNPs, unexpressed ab initio gene models, tRNAs, repeats raw genomic sequences alignments of three ribosomal genes (rpl9, rpl32, rpp1) used for phylogenetic tree reconstruction and conspecificity matrix generation H. hongkongensis and T. adhaerens reference coding sequences and alignments of 6,554 orthologs [fasta] H. hongkongensis and T. adhaerens reference protein sequences and alignments of 6,554 orthologs [fasta] H. hongkongensis (reference and allelic variants) and T. adhaerens (reference) coding sequences and alignments of 2,870 orthologs [fasta] H. hongkongensis (reference and allelic variants) and T. adhaerens (reference) protein sequences and alignments of 2,870 orthologs [fasta] Protein matrix used for distance calculations (dataset 1) [phylip] Alignments of selected single marker sequences for distance calculation (16S, cox1, nad1, 18S, 28S) [fasta] Protein alignments for 194 proteins used for phylogenetic inferences [fasta] Protein matrix used for phylogenetic inferences (dataset 2) [phylip] Dayhoff 6-state recoded protein matrix used for phylogenetic inferences (recoded dataset 2) [phylip] Partition files for dataset 1 & 2 [txt] Output files from Phylobayes and RAxML analyses Complete and annotated H. hongkongensis mitochondrial genome [gb, fasta].
Funding: LMUexcellent
https://www.en.uni-muenchen.de/about_lmu/research/excellence_initiative/index.html. Funding through the LMU Munich’s Institutional Strategy LMU excellent within the framework of the German Excellence Initiative to GW and HB. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Deutsche Forschungsgemeinschaft (DFG) www.dfg.de (grant number SCHI 277/26-1, SCHI 277/29-1). Funding to BS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The University of Hongkong. Funding through a Small Project Fund of The University of Hong Kong to GAW and ME (grant number 201109176175). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Studienstiftung des deutschen Volkes. Doctoral fellowship to HJO. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Deutscher Akademischer Austauschdienst (DAAD) www.daad.de. A postdoctoral research fellowship to M.E. that supported specimen collection and establishment of cultures. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. European Union’s Horizon 2020, Marie Skłodowska-Curie Innovative Training Networks
https://ec.europa.eu/research/mariecurieactions/actions/get-funding/innovative-training-networks_en (grant number 764840 [ITN IGNITE]). Funding to GW. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Deutsche Forschungsgemeinschaft (DFG) www.dfg.de (grant number Wo896/19-1). Funding to GW within the DFG Priority Program SPP 1991 “TaxonOMICs”. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: CDS, coding sequence; CM, conspecificity matrix; CO1, cytochrome c oxidase subunit 1; dN/dS, nonsynonymous to synonymous nucleotide substitutions; FPKM, fragments per kilobase million; GO, gene ontology; GPCR, G-protein coupled receptor; HMM, hidden Markov model; ITS2, internal transcribed spacer 2; MCL, Markov cluster; ND1, NADH dehydrogenase subunit 1; rDNA, ribosomal DNA; SNP, single nucleotide polymorphism; TPM, transcripts per kilobase million
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